Mineralized rods and cones suggest colour vision in a 300 Myr-old fossil fish

Tanaka, Gengo; Parker, Andrew R.; Hasegawa, Yoshikazu; Siveter, David J.; Yamamoto, Ryōichi; Miyashita, Kiyoshi; Takahashi, Yuichi; Ito, Shosuke; Wakamatsu, Kazumasa; Mukuda, Takao; Matsuura, Marie; Tomikawa, Ko; Furutani, Masumi; Suzuki, Kayo; Maeda, Haruyoshi

doi:10.1038/ncomms6920

Cited by 23 publications

(23 citation statements)

References 34 publications

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“…We suggested that the rounded elements in Triazeugacanthus specimens could be interpreted as eye lenses. The anterior morphological position in the head region, their rounded shape, the absence of mineralized tissues (C and O peaks), and the similarities with acanthodian, chondrichthyan and osteichthyan anatomy (this study, [45]) corroborate this interpretation.…”

Section: Chemical Composition Of Triazeugacanthus Biomineralized Tisssupporting

confidence: 74%

“…Thus, the rounded elements seen in Triazeugacanthus do not correspond to the orbit. Anterior paired rounded elements have been identified as the eyes of the Carboniferous acanthodian Acanthodes bridgei [45]. Rods and pigments, as well as molecules common only to eumelanine, were found in the dark brown fragments from these fossil eyes.…”

Section: Chemical Composition Of Triazeugacanthus Biomineralized Tissmentioning

confidence: 99%

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New Insights in the Ontogeny and Taphonomy of the Devonian Acanthodian Triazeugacanthus affinis From the Miguasha Fossil-Lagerstätte, Eastern Canada

2015

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Progressive biomineralization of a skeleton occurs during ontogeny in most animals. In fishes, larvae are poorly mineralized, whereas juveniles and adults display a progressively more biomineralized skeleton. Fossil remains primarily consist of adult specimens because the fossilization of poorly-mineralized larvae and juveniles necessitates exceptional conditions. The Miguasha Fossil-Lagerstätte is renowned for its Late Devonian vertebrate fauna, revealing the exceptional preservation of fossilized ontogenies for 14 of the 20 fish species from this locality. The mineralization of anatomical structures of the acanthodian Triazeugacanthus affinis from Miguasha are compared among larval, juvenile and adult specimens using Energy Dispersive X-ray Spectrometry. Chemical composition of anatomical structures of Triazeugacanthus reveals differences between cartilage and bone. Although the histology and anatomy is well-preserved, Fourier transform infrared spectrometry shows that the original chemical composition of bone is altered by diagenesis; the mineral phase of the bone (i.e., hydroxyapatite) is modified chemically to form more stable carbonate-fluorapatite. Fluorination occurring in mineralized skeletal structures of adult Triazeugacanthus is indicative of exchanges between groundwater and skeleton at burial, whereas the preservation of larval soft tissues is likely owing to a rapid burial under anoxic conditions. The exceptional state of preservation of a fossilized ontogeny allowed us to characterize chemically the progressive mineralization of the skeleton in a Devonian early vertebrate.

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Section: Chemical Composition Of Triazeugacanthus Biomineralized Tisssupporting

confidence: 74%

Section: Chemical Composition Of Triazeugacanthus Biomineralized Tissmentioning

confidence: 99%

New Insights in the Ontogeny and Taphonomy of the Devonian Acanthodian Triazeugacanthus affinis From the Miguasha Fossil-Lagerstätte, Eastern Canada

2015

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“…In terms of their consistent morphology and limited size range, the microbodies we describe closely resemble melanosomes in fishes [12,13] and amphibians [17]. Whether size and shape of microbodies is a reliable diagnostic feature to distinguish between fossil melanosomes and fossil bacteria is debated [18–20], but arguments that melanosomes and bacteria overlap in size, shape and preservation potential [21,22] are challenged by data demonstrating otherwise [18,23].…”

Section: Discussionmentioning

confidence: 99%

Pigmented anatomy in Carboniferous cyclostomes and the evolution of the vertebrate eye

et al. 2016

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The success of vertebrates is linked to the evolution of a camera-style eye and sophisticated visual system. In the absence of useful data from fossils, scenarios for evolutionary assembly of the vertebrate eye have been based necessarily on evidence from development, molecular genetics and comparative anatomy in living vertebrates. Unfortunately, steps in the transition from a light-sensitive ‘eye spot’ in invertebrate chordates to an image-forming camera-style eye in jawed vertebrates are constrained only by hagfish and lampreys (cyclostomes), which are interpreted to reflect either an intermediate or degenerate condition. Here, we report—based on evidence of size, shape, preservation mode and localized occurrence—the presence of melanosomes (pigment-bearing organelles) in fossil cyclostome eyes. Time of flight secondary ion mass spectrometry analyses reveal secondary ions with a relative intensity characteristic of melanin as revealed through principal components analyses. Our data support the hypotheses that extant hagfish eyes are degenerate, not rudimentary, that cyclostomes are monophyletic, and that the ancestral vertebrate had a functional visual system. We also demonstrate integument pigmentation in fossil lampreys, opening up the exciting possibility of investigating colour patterning in Palaeozoic vertebrates. The examples we report add to the record of melanosome preservation in Carboniferous fossils and attest to surprising durability of melanosomes and biomolecular melanin.

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“…Analytical techniques that detect biomolecules indicate that melanin granules occur in fossil cephalopods (25) and that melanin-bearing melanosomes are preserved in fossil fish (7,26) and marine reptiles (8). The most conclusive and comprehensive chemical study to date shows the presence of chemically intact melanin in quantities of ∼10% in Jurassic cephalopod ink sacs (25,27).…”

mentioning

confidence: 99%

Chemical, experimental, and morphological evidence for diagenetically altered melanin in exceptionally preserved fossils

Colleary

Dolocan²,

Gardner

et al. 2015

Proc. Natl. Acad. Sci. U.S.A.

101

163

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In living organisms, color patterns, behavior, and ecology are closely linked. Thus, detection of fossil pigments may permit inferences about important aspects of ancient animal ecology and evolution. Melanin-bearing melanosomes were suggested to preserve as organic residues in exceptionally preserved fossils, retaining distinct morphology that is associated with aspects of original color patterns. Nevertheless, these oblong and spherical structures have also been identified as fossilized bacteria. To date, chemical studies have not directly considered the effects of diagenesis on melanin preservation, and how this may influence its identification. Here we use time-of-flight secondary ion mass spectrometry to identify and chemically characterize melanin in a diverse sample of previously unstudied extant and fossil taxa, including fossils with notably different diagenetic histories and geologic ages. We document signatures consistent with melanin preservation in fossils ranging from feathers, to mammals, to amphibians. Using principal component analyses, we characterize putative mixtures of eumelanin and phaeomelanin in both fossil and extant samples. Surprisingly, both extant and fossil amphibians generally exhibit melanosomes with a mixed eumelanin/phaeomelanin composition rather than pure eumelanin, as assumed previously. We argue that experimental maturation of modern melanin samples replicates diagenetic chemical alteration of melanin observed in fossils. This refutes the hypothesis that such fossil microbodies could be bacteria, and demonstrates that melanin is widely responsible for the organic soft tissue outlines in vertebrates found at exceptional fossil localities, thus allowing for the reconstruction of certain aspects of original pigment patterns.

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Mineralized rods and cones suggest colour vision in a 300 Myr-old fossil fish

Cited by 23 publications

References 34 publications

New Insights in the Ontogeny and Taphonomy of the Devonian Acanthodian Triazeugacanthus affinis From the Miguasha Fossil-Lagerstätte, Eastern Canada

New Insights in the Ontogeny and Taphonomy of the Devonian Acanthodian Triazeugacanthus affinis From the Miguasha Fossil-Lagerstätte, Eastern Canada

Pigmented anatomy in Carboniferous cyclostomes and the evolution of the vertebrate eye

Chemical, experimental, and morphological evidence for diagenetically altered melanin in exceptionally preserved fossils

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